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Sparganosis Presenting As Cauda Equina Syndrome with Molecular Identification of the Parasite in Tissue Sections

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Sparganosis Presenting As Cauda Equina Syndrome with Molecular Identification of the Parasite in Tissue Sections ISSN (Print) 0023-4001 ISSN (Online) 1738-0006 Korean J Parasitol Vol. 51, No. 6: 739-742, December 2013 ▣ CASE REPORT http://dx.doi.org/10.3347/kjp.2013.51.6.739 Sparganosis Presenting as Cauda Equina Syndrome with Molecular Identification of the Parasite in Tissue Sections Adhiratha Boonyasiri1, Pornsuk Cheunsuchon2, Prajak Srirabheebhat3, Hiroshi Yamasaki4, 5,6 5,6, Wanchai Maleewong and Pewpan M. Intapan * 1Division of Infectious Diseases and Tropical Medicine, Department of Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand; 2Department of Pathology, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand; 3Division of Neurosurgery, Department of Surgery, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand; 4Department of Parasitology, National Institute of Infectious Diseases, Tokyo, Japan; 5Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand; 6Research and Diagnostic Center for Emerging Infectious Diseases, Faculty of Medicine, Khon Kaen University, Khon Kaen, 40002, Thailand Abstract: A 52-year-old woman presented with lower back pain, progressive symmetrical paraparesis with sensory im- pairment, and sphincter disturbance. Magnetic resonance imaging (MRI) of the whole spine revealed multiple intradural extramedullary serpiginous-mass lesions in the subarachnoid space continuously from the prepontine to the anterior part of the medulla oblongata levels, C7, T2-T8, and T12 vertebral levels distally until the end of the theca sac and filling-in the right S1 neural foramen. Sparganosis was diagnosed by demonstration of the sparganum in histopathological sections of surgically resected tissues and also by the presence of serum IgG antibodies by ELISA. DNA was extracted from unstained tissue sections, and a partial fragment of mitochondrial cytochrome c oxidase subunit 1 (cox1) gene was amplified using a primer set specific for Spirometra spp. cox1. After sequencing of the PCR-amplicon and alignment of the nucleotide sequence data, the causative agent was identified as the larva of Spirometra erinaceieuropaei. Key words: Spirometra erinaceieuropaei, sparganosis, cauda equina syndrome, molecular identification INTRODUCTION identification of the causative agent and review the literature of sparganosis involving the spinal cord. Human sparganosis is a zoonosis caused by plerocercoid larvae (=spargana) of pseudophyllidean (now classified as di- CASE RECORD phyllobothriidean [1,2]) tapeworms [3,4]. In Asia, S. erinacei- europaei is responsible for this disease, whereas Spirometra man- The patient was a 52-year-old female sugarcane farmer who sonoides is important in the Americas. Sparganosis usually ap- lived in a rural community of Suphan Buri Province, central pears as slowly growing and migratory subcutaneous nodules. Thailand. She presented to our hospital complaining of lum- This parasite can be found anywhere in the body including the bodorsal pain for the previous month, progressive symmetri- central nervous system [5,6]. In rare cases, a sparganum involves cal paraparesis with sensory impairment and radiculopathy for the spinal cord, usually at the thoracic to lumbar levels [7-15]. 2 weeks, and bowel/bladder dysfunction for 3 days. She had To our knowledge, only 3 cases have been reported as sparga- no history of ingesting inadequately cooked frogs, snakes, or nosis with cauda equina syndrome [11,14,16]. None of these birds. On examination, the patient had a normal body tem- cases were confirmed by molecular diagnosis. Here, we describe perature. Skin nodules or organomegaly was not observed. a case of cauda equina syndrome with molecular evidence for Mental status and cranial nerve functions were within normal limits. Neurological examinations revealed decreased motor Received 30 May 2013, revised 25 July 2013, accepted 11 October 2013. tone of both legs. Motor strength of the left lower extremity • Corresponding author ([email protected]) * decreased from grade V (normal) to grade III in the hamstrings, © 2013, Korean Society for Parasitology and Tropical Medicine iliopsoas, and quadriceps muscles; grade I-II in the ankle and This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) toe plantar flexor muscles; and grade 0 in the ankle dorsiflex- which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. ors muscles and the extensor hallucis longus muscle. For the 739 740 Korean J Parasitol Vol. 51, No. 6: 739-742, December 2013 HRA PC HRA T12 T12 L1 L1 S1 S1 A B A 50 μm B 20 μm Fig. 1. Magnetic resonance of lumbosacral spine sagittal T2W image (A) and sagittal T2W with fat suppression image (B) shows Fig. 2. Histopathological findings of the resected lesion. (A) Section abnormal lower lumbar spinal cord, conus medullaris, and cauda of a degenerating cestode larva (molecular confirmed as Spirome- equina. Multiple heterogeneously serpigineous lesion filling within tra erinaceieuropaei) with homogenously eosinophilic and irregularly T12 to S1 of the thecal sac. ridged tegument. Calcareous bodies and inflammatory cell infiltra- tions are seen throughout the parasite body. ×200. (B) Calcareous bodies (arrows) and mild inflammatory cell infiltrations including right lower extremity, motor strength was decreased to grade lymphocytes and a few eosinophils, plasma cells, and polymor- III in all the muscles. Sensations were decreased below the L2 phonuclear cells are seen in the body of the cestode larva. ×400. dermatome on both sides with peri-anal anesthesia, and the knee and ankle jerk were absent on both sides. Anal sphincter lymphocytes, a few plasma cells, and neutrophils in the larval tone was reduced. A clinical diagnosis of cauda equina syn- section (Fig. 2). The definite diagnosis of sparganosis could be drome was made. Routine biochemical and hematological in- made from the histopathological findings. vestigations were within normal limits except for an increase of After the histopathological confirmation, serological tests absolute eosinophil count in the peripheral blood (0.46 ×109/L). for detection of specific antibodies in the serum was performed. MRI of the whole spine showed multiple intradural extramed- Using ELISA, we detected a high titer of specific IgG antibodies ullary serpiginous-mass lesions in the subarachnoid space against S. erinaceieuropaei sparganum partially purified antigen. continuously from the prepontine to the anterior part of the The serum was negative for cysticercosis by ELISA and also medulla oblongata levels, C7, T2-T8, and T12 vertebral levels negative for gnathostomiasis, paragonimiasis, fascioliasis, and distally until the end of the thecal sac, and filling-in of the angiostrongyliasis by immunoblotting. right S1 neural foramen (Fig. 1). Attempts of spinal tapping to For molecular identification of the causative parasite species, obtain a cerebrospinal fluid (CSF) sample were unsuccessful. DNA was extracted from 10 μm unstained serial sections (cut Laminectomy at L1 and L2 level was performed to obtain a from the formalin-fixed paraffin-embedded specimen) attached tissue sample for histopathological examinations. During the to glass slides using a DEXPAT kit (TaKaRa Bio Inc., Tokyo, Ja- operation, we noticed a matted mass involving nerve roots pan) as reported previously [17]. The resulting supernatants with remarkable inflammation and multiple cystic lesions were used as the DNA template for PCR. Amplification of mi- containing pus; no CSF was seen due to obstruction by the tochondrial cytochrome c oxidase subunit 1 (cox1) gene by mass. A small piece of tissue from the matted mass was re- PCR was performed in a 25 μl reaction mixture. A fragment of moved and fixed in formalin and processed for paraffin em- cox1 gene was amplified using the primers Se658-F (5´-TTT GAT bedding. The histological sections were stained with hematox- CCT TTG GGT GGT GG-3´) and Se1124-R (5´-ACC ACA AAC ylin and eosin. Histological examinations demonstrated a de- CAC GTG TCA TG-3´), which were designed from the cox1 gene generated solid section of a folded cestode larva having irregu- of S. erinaceieuropaei (GenBank accession no. AB369250). PCR lar folding tegument which was homogenously eosinophilic was carried out using a GeneAmp PCR System 9700 (Applied in color. Many calcareous corpuscles (Fig. 2B arrows), which is Biosystems, Singapore). The reaction was carried out in a 25 µl a characteristic feature of a cestode larva, were seen. There were volume containing 2.5 µl of 10x FastStart High Fidelity Reac- mild inflammatory cell infiltrations including eosinophils, tion buffer with 18 mM MgCl2 (Roche, Mannheim, Germany), Boonyasiri et al.: Sparganosis presenting as cauda equina syndrome 741 200 μM of each deoxyribonucleotide triphosphate, 0.2 μM of volved intradural (70%) than extradural [8,9,15] sites, usually each primer (Invitrogen, Carlsbad, California, USA), and 0.625 at the thoracic level [7-10,12,13], followed by the cervical level units of FastStart High Fidelity Enzyme Blend (Roche). The [9]. Including the present case, there were only 3 cases of spar- DNA template was initially denatured at 94˚C for 5 min. The ganosis involving the conus medullaris and cauda equina amplification procedure consisted of 35 cycles at 95˚C for 30 [13,14]. Our patient demonstrated long
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